Download survey of inorganic arsenic in seaweed and seaweed

SURVEY OF INORGANIC ARSENIC IN SEAWEED AND
SEAWEED-CONTAINING PRODUCTS AVAILABLE IN
AUSTRALIA
Executive summary
Food Standards Australia New Zealand (FSANZ) conducted a small survey investigating levels of
inorganic arsenic in dried seaweed and products containing seaweed available in Australia. This
survey was conducted as part of the FSANZ surveillance and monitoring program in 2010 with the
intention of reviewing our consumer advice released in 2004. In November 2004, FSANZ issued a
media release advising Australian consumers to avoid hijiki seaweed as it may contain high levels
of naturally occurring inorganic arsenic.
The levels of inorganic arsenic in various seaweed types tested were all below the maximum level
(ML) for seaweed of 1 mg/kg in the Australia New Zealand Food Standards Code (the Code), with
the exception of one composite sample of hijiki seaweed. The details of the hijiki seaweed were
referred to the relevant jurisdiction for further investigation and/or any relevant follow-up activity.
High inorganic arsenic concentrations in hijiki seaweed are consistent with findings in other
countries. The levels of inorganic arsenic in products containing seaweed (e.g. seaweed chips)
were comparable with the levels reported for similar foods in other countries.
Inorganic arsenic survey results were combined with results from the 23rd Australian Total Diet
Study (ATDS) to estimate total inorganic arsenic dietary exposure. In general, consumption of
seaweed and seaweed products in the Australian population is likely to be low and the resulting
contribution to total dietary inorganic arsenic exposure is therefore likely to be small for the general
population. Population groups or individuals that have a high exposure to arsenic from other
sources in the diet, and who also regularly consume hijiiki seaweed, should be aware that they
may have a higher potential health risk from arsenic than the general population. FSANZ has
therefore reviewed and updated the factsheet for consumers regarding seaweed, which is
available on the FSANZ website.
The findings from this survey indicate that the majority of samples tested demonstrated compliance
with the requirements in the Code, with the exception of one composite sample of Hijiki. This high
level of compliance is consistent with the monitoring conducted by the Department of Agriculture,
Fisheries and Forestry (DAFF) at the border.
FSANZ will continue to monitor arsenic levels in food through the ATDS. The next ATDS (the 25th
study) will investigate arsenic levels, including inorganic arsenic, in a range of foods commonly
consumed in the typical Australian diet.
2
1 Background
In November 2004, FSANZ issued a media release advising Australian consumers to avoid hijiki
seaweed as it may contain high levels of naturally occurring inorganic arsenic. This was based on
advice obtained from the United Kingdom (UK) where the Food Safety Authority (FSA) reported
high levels of inorganic arsenic in hijiki seaweed (FSA 2004). At the time, FSANZ provided risk
assessment advice to the Department of Agriculture, Fisheries and Forestry (DAFF) (formerly
Australian Quarantine and Inspection Service) that inorganic arsenic levels above 1 mg/kg were
considered a medium to high risk. This advice to DAFF resulted in the testing of all imported hijiki
seaweed for inorganic arsenic. This was to ensure that levels did not represent an unacceptable
risk to public health and safety.
FSANZ regularly monitors the food supply for levels of substances in food. Given the consumer
advice issued in 2004 about high levels of inorganic arsenic in certain seaweeds, a survey on
inorganic arsenic in seaweed was included in FSANZ’s monitoring and surveillance program for
2010 with the intention of reviewing the consumer advice released in 2004.
1.1 Seaweed
Seaweed is a type of algae commonly harvested from cold, tropical and temperate waters.
Seaweed species are diverse and are generally classified into three separate phyla based on
colour and other characteristics (FAO 2003; Gupta and Abu-Ghannam 2011). These are:



brown seaweed from Phaeophyceae, which includes Laminaria spp., Undaria spp. and
Hizikia (also known as hijiki) spp. These species are commonly used in salads, soups and
stir-fries.
red seaweed from Rhodophyceae, which includes laver, nori and dulse. Nori is commonly
used in sushi and dulse is used as a condiment.
green seaweed, from Chlorophyceae which includes the Ulva spp., (sea lettuce is derived
from this species).
Seaweed bioaccumulates available elements from the environment such as sodium, potassium,
chloride, magnesium, calcium, phosphorus, iron, manganese, zinc, copper, chromium, selenium
and iodine (Almela et al 2002; Gupta and Abu-Ghannam 2011; Dawczynski et al 2007; Smith et al
2010). While seaweed contains a number of elements with nutritional properties, it also
accumulates some heavy metal contaminants including inorganic arsenic that may raise health
concerns, depending on the level of exposure (Dawczynski et al. 2007; Hwang et al. 2010; Smith
et al. 2010; Almela et al. 2002; Almela et al. 2006). Hijiki1 seaweed, in particular, can accumulate
very high levels of arsenic under certain circumstances. The level of individual elements varies in
seaweed and is influenced by the species of seaweed, source, season, temperature and method of
harvesting (Borak and Hosgood 2007).
1.2 A focus on arsenic
Arsenic is a metalloid that occurs in different inorganic and organic forms, which are found in the
environment both from natural occurrence and from anthropogenic (human) activity (WHO 2011a).
While individuals are often exposed to both organic and inorganic arsenic through the diet, it is the
inorganic species (which include arsenate V [Asv] and arsenite III [AsIII])2 that are considered to be
1
The term ‘hijiki seaweed’ can be used to refer to unprocessed harvested seaweed which is then dried, or processed
product which has been boiled with other brown seaweed types, dried and packaged. For the purpose of this
report, Hijiki encompasses both forms unless otherwise indicated in published research papers.
2
Several arsenic species occur in food. Monomethylarsonic acid (MMA), and dimethylarsinic acid (DMA) are organic
species of arsenic with toxicological significance. Inorganic arsenic is usually reported as the sum of arsenite and
arsenate.
3
more toxic to humans than organic arsenic. Only inorganic arsenic is known to be carcinogenic in
humans. Inorganic arsenic contamination of groundwater is common in certain parts of the world.
Dietary exposure to inorganic arsenic occurs predominantly from groundwater derived drinkingwater, groundwater used in cooking and commonly consumed foods such as rice and other cereal
grains and their flours (EFSA 2009; WHO 2011a).
Seafood is a major contributor to total (inorganic plus organic) arsenic dietary exposure and was,
for example, estimated to contribute to approximately 90% of exposure in the United States (US)
(Borak and Hosgood 2007). The predominant species of arsenic in seafood is, however, the less
toxic organic form, with a minor contribution from the more toxic, inorganic species (Borak and
Hosgood 2007). Arsenic is also found in fruits and vegetables at parts per billion concentrations,
predominantly in the inorganic forms (Norton et al 2012). Seaweed contains higher inorganic
arsenic levels as a proportion of the total arsenic (e.g. 60-73%; Almela et al 2002; Rose et al 2007)
than many other foods. Given the diversity in the range of seaweed species available, the levels of
inorganic arsenic also vary. Specific types of seaweed such as hijiki, have been found to
consistently contain higher levels of inorganic arsenic than other types (Almela et al 2002; Rose et
al 2007).
1.3 Risk management measures in Australia, New Zealand and in other countries
The Australia New Zealand Food Standards Code (the Code) includes a maximum limit (ML) for
inorganic arsenic in seaweed. Standard 1.4.1 – Contaminants and Natural Toxicants contains a ML
for inorganic arsenic of 1 mg/kg, calculated with respect to the mass of seaweed at 85% hydration.
In general, MLs are established for contaminants in those foods which are significant contributors
to the overall dietary exposure for the particular contaminant. A ML for inorganic arsenic in
seaweed was maintained when the Code was reviewed to harmonise the regulation of metal
contaminants in food between Australia and New Zealand through Proposal P157 – Contaminants
in Foods. The ML for inorganic arsenic in seaweed was expected to be highly protective of
consumers (ANZFA 1999). While a ML is set for inorganic arsenic in seaweed, the general
principle of keeping levels of contaminants in food As Low As Reasonably Achievable (ALARA)
applies, particularly given the carcinogenic nature of inorganic arsenic. The majority of seaweed is
imported into Australia and therefore a large proportion of the seaweed sold in Australia will have
been monitored at the border by DAFF for compliance with the Code.
Standard 1.4.1 of the Code also includes a formula for determining the appropriate ML to apply to
mixed foods that takes into account the proportion of each individual food within the mixed food.
The formula can be used to determine the appropriate ML for inorganic arsenic in foods containing
seaweed as an ingredient, if the proportion of each ingredient is known.
Food regulatory counterparts in other countries have not established specific maximum limits for
inorganic arsenic in seaweed; however limits have been set for total arsenic. For example, in the
UK there is a limit of 1 mg/kg of total arsenic in food, although this level specifically excludes
seaweed. In 2004, the UK Food Standards Agency (FSA) issued a warning to consumers to avoid
consumption of hijiki seaweed based on survey findings of total arsenic and inorganic arsenic in
five imported seaweed species (FSA 2004). The FSA repeated this message in 2010, after
identifying a brand of hijiki seaweed with high levels of inorganic arsenic (FSA 2010). Similarly, the
Canadian Food Inspection Agency (CFIA), has taken an advisory approach, recommending that
hijiki seaweed consumption is avoided due to the potential health risks (CFIA 2010).
1.4 Monitoring dietary exposure to arsenic from the food supply
FSANZ has been monitoring the dietary exposure of the Australian population to total arsenic for a
number of years through the Australian Total Diet Study (ATDS) with results reported in the 19th,
20th and 23rd ATDS (FSANZ 2001a, FSANZ 2003, ANZFA 2001, see Section 5.2). The majority of
foods contained quantifiable concentrations of arsenic in at least one of the samples analysed,
however inorganic arsenic was only measured in seafood. The contribution of seaweed to the
4
overall dietary exposure to total arsenic was not captured in these studies as it was not considered
to be a food commonly consumed in a typical Australian diet.
2 Objectives
The objectives of this survey were to:



determine the concentration of inorganic arsenic in a variety of seaweed types and
seaweed-containing products available in Australia
describe any additional health and safety risks associated with increased exposure to
inorganic arsenic from seaweed consumption
review the consumer advice issued in 2004 based on the findings of this study, and revise if
appropriate.
3 Methodology
3.1 Sampling
The samples used for inorganic arsenic analysis were selected from the range of seaweed and
seaweed products that had already been sampled for the Survey of iodine in seaweed and
seaweed containing products (FSANZ, 2011b). These samples were collected from a variety of
retail outlets in April/May 2010 from all states and territories in Australia.
A total of 38 individual samples of seaweed and seaweed products were investigated in this
survey. From these samples, the analyses conducted were:




Twenty two (22) individual samples.
Three (3) composites comprising three primary samples (individual purchases) of different
brands.
One (1) composite comprising three primary samples (individual purchases) of the same
brand.
Two (2) composites comprising two primary samples (individual purchases) of the same
brand.
Composite samples comprised of the same type of seaweed (e.g. wakame) based on the
ingredients list, or the same type of product (e.g. miso paste) with varying use-by dates/batch
codes.
3.2 Sample preparation
All seaweed samples were analysed in a dried state, directly from the packaging. Seaweed
containing products, including soup and tea, were analysed by the laboratory as purchased.
3.3 Analysis
FSANZ engaged the National Measurement Institute (NMI) to analyse the samples for total
inorganic arsenic using a NATA accredited method of acid extraction followed by Hydride
Generation Inductively Coupled Plasma-Mass Spectrometry (ICP-MS) (Holak and Specchio 1991).
The Limit of Reporting (LOR) was 0.05 mg/kg with a Practical Quantitation Limit (PQL) of 0.03
mg/kg. The PQL is equivalent to the Limit of Quantification (LOQ) and is reported by some
laboratories instead of the LOQ. In this survey, the LOR is slightly higher than the PQL, to account
for matrix variations in the samples analysed.
Total inorganic arsenic in this report is defined as total arsenite (As3+) and arsenate (As5+).
Because of the extraction method used, it is possible that total inorganic arsenic detected may also
contain some low levels of monomethylarsenate (MMA) which is an organic form of arsenic with
5
toxicological significance. For the purposes of this report, a conservative approach has been taken
and the possible presence of organic MMA has been included in the total inorganic arsenic
concentration.
All analytical concentration values for inorganic arsenic presented in this report are from dried
seaweed rather than the 85% hydrated form, unless otherwise specified. The inorganic arsenic
concentration in the 85% hydrated form was calculated only for the sample where the level in the
dried seaweed was above the ML in the Code to enable the analytical concentrations to be
compared with the ML on the same basis.
For the purposes of calculating mean and median concentrations of inorganic arsenic in seaweed
and food containing seaweed (Table 1 and 2), samples reported as <LOR of 0.05 mg/kg were
assumed to be 0.05 mg/kg. This is known as the upper bound estimate and is a conservative
approach since it is more likely to overestimate rather than underestimate the true mean arsenic
concentration of the samples analysed.
4 Results
A summary of the results is provided in Table 1 and Table 2.
For samples of dried seaweed, inorganic arsenic levels were reported above the LOR of 0.05
mg/kg for all samples except one (seaweed type not specified). Concentrations ranged from <0.05
mg/kg in an unspecified type of seaweed to 7.8 mg/kg in dried hjijki. In general, inorganic arsenic
concentrations were higher in wakame, kombu, hijiki and Sargassum fusiforme in comparison to
levels detected in nori, unspecified types of seaweed and sea vegetables.
For seaweed containing products, inorganic arsenic concentration was reported above the LOR for
only two samples (seaweed chips). The concentration of inorganic arsenic in these chip samples
was similar to levels detected in some seaweed types (e.g. nori, unspecified types of seaweed).
The difference between the inorganic arsenic in dried seaweed and seaweed containing products
may simply reflect the proportion of seaweed in the final product.
6
Table 1 Inorganic arsenic concentration (mg/kg) in individual and composite samples of dried
seaweed
Seaweed type
(as indicated on
product packaging)
Wakame (dried)
Kombu (dried)
Hijiki (dried)
Sargassum fusiforme
(dried)
Nori (dried)
Seaweed, type not
specified (dried)
Sea vegetable (dried)
†
Overall Mean
Overall Median
Minimum
Maximum
Inorganic arsenic
concentration (mg/kg)†
0.19
0.20
0.16
0.16β
0.33
0.19
0.18
0.16
7.80‡
Mean inorganic
arsenic
concentration
(mg/kg)∞
0.18
0.22
n/a
0.32¥
n/a
0.16€
0.09
0.10
0.09
0.12
<0.05 (0.05 upper bound)
0.10β
0.11
0.61
0.16
0.05 (upper bound)
7.80
0.09α
n/a
n/a
n/a
n/a
n/a
Concentration values are for individual samples unless otherwise indicated.
Composite sample comprised 3 primary purchases (individual samples) of different brands.
‡
Concentration value is from a composite sample comprising 2 primary purchases (individual samples) of the same brand
of product.
¥
Concentration value is from a composite sample comprising 2 primary purchases (individual samples) of different brands.
€
Concentration value is from a composite sample comprising 3 primary purchases (individual samples) of the same brand
of product.
∞
The mean has been rounded to two decimal places.
n/a: not applicable.
α
To calculate the mean for this sample the upper bound was used (non-detect results assigned value of 0.05 mg/kg).
β
7
Table 2 Inorganic arsenic concentration (mg/kg) in individual and composite samples of products
containing seaweed.
Products containing seaweed
(as purchased)
Total Inorganic arsenic
†
concentration (mg/kg)
β
Miso soup (dried)
<0.05
Seasoning sauce (as purchased)
<0.05
<0.05
<0.05
<0.05
0.14
0.11
<0.05
<0.05
<0.05
<0.05
Seaweed chips
Desserts containing seaweed
(as purchased)
Japanese tea (dried)
Mean concentration for total
‡
inorganic arsenic (mg/kg)
n/a
0.05
(upper bound)
0.10
0.05
(upper bound)
n/a
†
Concentrations are for individual samples unless otherwise indicated.
samples were analysed as a composites comprising 3 primary purchases (individual samples) of different brands.
‡
For the purpose of calculating the mean, values reported at or below the LOR have been assumed to be the LOR of
0.05 mg/kg (upper bound). The mean has been rounded to two decimal places.
n/a: not applicable.
β
4.1 Comparing inorganic arsenic levels in dried seaweed with permissions in the Code
The results from this survey indicate that arsenic levels in dried seaweed samples were well below
the ML for seaweed of 1 mg/kg (see section 1.3) with the exception of one composite sample of
dried hijiki seaweed for which an inorganic arsenic concentration of 7.8 mg/kg (equivalent to 1.4
mg/kg at 85% hydration)3 was reported.
For mixed foods that contain seaweed as an ingredient, a formula is included in the Code to
calculate an appropriate ML to apply for comparative purposes, based on the proportion of each
ingredient in the final product (see section 1.3). However, since the samples used in this survey
were purchased from retail outlets, some of the information required to calculate the appropriate
MLs for these mixed foods was not available. For example, in some cases the proportion of
seaweed in the mixed food was not indicated on the label.
4.2 Comparing inorganic arsenic concentrations determined from this survey with levels
reported in other countries
The high level of inorganic arsenic in hijiki seaweed in comparison to other seaweeds is consistent
with previous studies. For example, a study conducted by Almela et al. (2006) determined the
concentration of inorganic arsenic in a variety of seaweed types available in Spain. The study
found that inorganic arsenic levels in Hizikia fusiforme were at least 27-fold higher in comparison to
other brown seaweed types, and 47-fold and 115-fold higher in comparison to red and green
seaweed samples, respectively. In the current survey, the inorganic arsenic level in hijiki seaweed
was at least 23-fold higher than the other brown seaweed samples tested and approximately 48fold higher than the red seaweed, nori.
A comparison of inorganic arsenic levels in seaweed species in a number of countries is provided
in Table 3. The concentration of inorganic arsenic in wakame, kombu and nori seaweed is similar
in the various countries. Evidently, in all countries represented in Table 3, the concentration of
3
This calculation is based on a moisture content of 14.6% as determined from this survey in a second sample of the
same dried hijiki seaweed composite.
8
inorganic arsenic in hijiki seaweed was the highest, ranging from 7.8 mg/kg in Australia to 117
mg/kg in Spain (Almela et al. 2006).
Table 3 A comparison of inorganic arsenic concentration in seaweed species in various countries
Inorganic arsenic concentration (mg/kg)
Seaweed
Type
(dried)
FSANZ
2012
N=38
NSWFA
2010¥
N=48
Almela
et al 2002Ω
N=18
AUSTRALIA*
Wakame
Kombu
Hijiki/
Sargassum
fusiformeπ
Nori
Sea
vegetable
0.16 - 0.20
0.16 - 0.33
0.06 –
0.51
<0.05 0.52
Almela
et al 2006£
N=112
SPAIN∞
FSA,
2004;
Rose et al
2007†
N=31
Smith
et al
2010α
N=10
UK€
NEW
ZEALAND
0.15 - 0.26
<LD -1.12
<0.3
0.1
0.254 0.297
0.238 -1.44
<0.3
n/a
0.32 - 7.8
n/a
83 - 85
41.6-117
77
n/a
0.09 0.16€
0.08 - 0.39
0.19 - 0.57
0.116 0.402
<0.3
1.2‡
0.10
0.13 - 0.23
n/a
n/a
n/a
n/a
†
Mean values are presented.
value presented is for Porphyra;
¥
values presented represent the range of values from various samples tested.
Ω
fresh hijiki was dried prior to analysis.
£
seaweed type is listed as Hizikia fusiforme; LD = limit of detection.
*
The Limit of Reporting (LOR) for both studies is 0.05 mg/kg;
∞
the LOR for both studies is 0.014 mg/kg;
€
LOR for both studies is 0.3 mg/kg;
α
LOR is not reported.
n/a not applicable
π
Hijiki samples are as purchased from retail outlets. The status of hijiki processing prior to packaging is unknown (see
footnote 1)
‡
A comparison of inorganic arsenic levels in products containing seaweed with similar products in
other countries is difficult due to the limited number of published studies in this area. Almela et al
(2006) determined the concentration of inorganic arsenic in red miso soup and tisane (herbal tea)
to be 0.05 mg/kg and 0.610 mg/kg, respectively (dry weight). These levels are comparable to those
determined in this study, which reported inorganic arsenic levels at or below the LOR of 0.05
mg/kg for both miso soup and tea.
5 Risk assessment
5.1 Hazard assessment
Inorganic arsenic is a carcinogen in humans (WHO, 2011a). In 2010, the Joint FAO/WHO Expert
Committee on Food Additives (JECFA) re-considered the existing health-based guidance value for
inorganic arsenic using a benchmark dosing model approach. The inorganic arsenic lower limit on
the benchmark dose for a 0.5% increased incidence of lung cancer (BMDL0.5) was determined from
epidemiological studies to be 3 μg/kg body weight per day (bw/day) (2–7 μg/kg bw/day based on
the range of estimated total dietary exposure) using a range of assumptions to estimate total
dietary exposure to inorganic arsenic from drinking-water and food (; WHO 2011a). Uncertainties in
9
this BMDL0.5 relate to assumptions regarding total exposure and to extrapolation of the BMDL0.5 to
populations other than those in Asia, where the epidemiological studies were undertaken, due to
the uncertainties around the influence of nutritional status, such as low protein intake, and other
lifestyle factors on the observed outcomes. JECFA noted that the existing health-based guidance
value, namely the provisional tolerable weekly intake (PTWI) of 15 μg/kg bw (equivalent to 2.1
μg/kg bw/day) was in the region of the BMDL0.5 and therefore was no longer appropriate and the
PTWI was withdrawn.
JECFA recommended that future epidemiological studies of the health impacts of arsenic should
incorporate appropriate measures of total exposure to inorganic arsenic, including from food,
drinking water and from water used in cooking and processing of food. It was further recommended
that epidemiological studies not only focus on relative risks, but also analyse and report the data
such that they are suitable for estimating exposure levels associated with additional (lifetime) risks,
so as to make their results usable for quantitative risk assessment.
5.2
Estimated dietary exposure to total arsenic and inorganic arsenic
5.2.1 Australian Total Diet Study
In the 19th, 20th and 23rd ATDS, total arsenic (sum of inorganic and organic species) concentrations
were determined in all foods commonly consumed in a typical Australian diet. The estimated mean
dietary exposure to total arsenic in the 23rd ATDS was 0.4-1.4 μg/kg bw/day, dependent on the
population groups being assessed (FSANZ 2011a). Results consistent with this were reported for
the previous 19thand 20th ATDS (ANZFA 2001; FSANZ 2003). In the 23rd ATDS, the estimated 90th
percentile dietary exposures to total arsenic for each age group were between 1.0 and
2.8 µg/kg bw/day for the lower bound4, and between 1.2-3.2 µg/kg bw/day for the upper bound5
estimates. The major contributors to dietary exposure were seafood and cereal and grain based
foods, consistent with those reported in other countries (EFSA 2009, WHO 2011 a and b).
Comparison of arsenic exposure between Australia and other countries is difficult because of major
differences in consumption patterns, regional geology and the amount of arsenic present in
drinking water. Broadly speaking, total arsenic exposure in Australia is at the lower end of the
range of exposures reported in comparable countries and regions, such as the US and the
European Union (EU). However, it should be noted that even within countries, the exposure to
arsenic between localised populations can vary substantially (see section 5.2.3 below).
In the 23rd ATDS, inorganic arsenic concentrations were also determined in a range of seafood
samples that are considered to be commonly consumed in Australia (e.g. battered fish fillets,
frozen fish portions, tuna canned in brine and cooked prawns). Seaweed and seaweed products
were not included in the 23rd ATDS. All samples analysed for inorganic arsenic were reported to
be below the LOR of <0.05 mg/kg.
5.2.2 Estimated additional dietary exposure to arsenic from seaweed
This survey has found that some seaweeds are a potential source of arsenic exposure that had not
been included in the dietary exposure estimates for total arsenic in the 23rd ATDS.
Using the dietary exposure estimates from the 23rd ATDS as a baseline, FSANZ considered a wide
range of possible scenarios to describe potential additional dietary exposure to inorganic arsenic
for individual consumers of seaweed based food. Based on FSANZ’s understanding of current
typical Australian consumption patterns, seaweed is unlikely to be widely or regularly consumed by
very young children and across the wider population, with the possible exception of sushi nori. In
the absence of consumption data from national nutrition surveys for seaweed and seaweed
products at an individual level, FSANZ assumed that all population groups would consume the
equivalent of 10 g of dried seaweed per day, an amount that is likely to be an upper level of
4
5
Lower bound assumes that where no arsenic was reported it is not present in the food
Upper bound assumes that where no arsenic was reported it was present at the limit of reporting
10
consumption. Appendix 1 describes the scenarios in detail, shows the related inorganic arsenic
exposure estimates and clearly identifies the assumptions and uncertainties of the dietary
exposure estimates.
For the ‘best case’ scenario, potential inorganic arsenic exposure from all food sources ranged
from 0.3-0.7 µg/kg bw/day; for the worst case scenario, from 2.2 to 7.6 µg/kg bw/day. For the
population group aged 2-5 years, exposure varied from 0.7-7.6 µg/kg bw/day, depending on the
scenario. For 6-12 year olds and 13-16 year olds exposure varied from 0.5-4.2 µg/kg bw/day and
0.3-2.7 µg/kg bw/day respectively. For adults, the range was 0.3 - 2.2 µg/kg bw/day.
Overall, dietary exposure estimates show that daily consumption of seaweed has only a minor
impact on overall inorganic arsenic exposure when the concentrations of inorganic arsenic is at the
median level for seaweed, as determined in this survey. If the highly protective assumption is made
that all the seaweed consumed contains inorganic arsenic at the maximum level reported in this
survey, this (not unexpectedly), results in substantially increased exposure estimates across all
population groups (worst case scenario). However, it is noted that this is unlikely to occur in reality
as arsenic concentration in seaweed covers a wide distribution of values and only some population
sub groups or individuals will consume seaweed and seaweed products on a daily basis with many
consuming less than 10 g dried seaweed a day.
5.2.3
Dietary exposure reported in the literature for countries other than Australia
It is often difficult to compare exposure estimates on total and inorganic arsenic between studies
and between countries. It is important to note that drinking water is the major contributor to arsenic
exposure in certain regions of some countries, but that this is not always included in dietary
exposure estimates. Inorganic arsenic exposure estimates, if reported, are often not based on
direct analyses, but derived by applying different factors to total arsenic results for different foods
to represent the proportion that is likely to be inorganic arsenic. These factors may vary between
studies.
A comprehensive review of dietary exposure estimates for different countries was undertaken by
Uneyama et al. (2007). They reported the following daily total arsenic exposures which are
represented in Table 4.
Table 4 A comparison of estimated inorganic arsenic intake in various countries‡
Region
Minimum (µg/day)
Maximum (µg/day)
0.001
Portugal
27
Japan
458
Spain
658
India
USA
7
137
Canada
6
38.1
New Zealand
n/a
55
South America
6.9
Brazil
145
Brazil
Europe
Asia
‡
Estimated inorganic arsenic exposure
Information taken from Uneyama et al, 2007.
Watanabe et al (2004) reported mean exposure to total arsenic in Bangladesh at 13.48 (men) and
10.30 (women) μg/kg bw/day and Kile et al (2007) reported 0.91 μg/kg bw/day. The large
11
differences in exposure were due to the assumptions on the level of arsenic in drinking water made
in the first study.
Diaz et al (2004) report that the mean total arsenic exposure in Chile ranged from 0.63-1.1 μg/kg
bw/day for food only and from 2.18 to 23.3 μg/kg bw/day where water was included in the
estimates.
Leblanc et al (2000) and Sirot et al (2009) estimated the mean exposure to total arsenic in French
populations. Leblanc et al (2000) reported mean exposure for the whole French population at 1.82
μg/kg bw/day from the French Total Diet Study, which did not include drinking water in the
estimates. The Sirot et al (2009) study was on a coastal population where fish and seafood
consumption was higher than elsewhere; mean exposure to total arsenic was reported to be 11.0413.53 μg/kg bw/day and the 95th percentile to be 25.14-33.0 μg/kg bw/day. Drinking water was
included in their exposure estimate.
Tsuda et al (1995) and Ogawa and Kayama (2009, as quoted by WHO 2011b) reported that the
mean exposure to total arsenic for Japanese populations was 3.82-4.73 μg/kg bw/day and 19.7124.10 μg/kg bw/day respectively. Ogawa and Kayama (2009, as quoted by WHO 2011b) focused
their estimates on fish and rice growing communities that were high consumers of seaweed, fish
and shell fish. They also reported 95th percentile and maximum exposures: 68.86-78.00 μg/kg
bw/day and 114.00-159.57 μg/kg bw/day respectively. In contrast, they reported that the mean
exposure for the whole Japanese population (based on a Total Diet Study) was estimated at 4.914.96 μg/kg bw/day.
The European Food Safety Authority (EFSA) (2009) reported a wide range of exposure estimates
in European countries. For example, lower bound exposures for total arsenic reported across 19
European countries ranged from 0.4 to 4.3 μg/kg bw/day at the mean of exposure (0.6-4.5
μg/kg bw/day for the upper bound) and from 1.8 to 11.0 μg/kg bw/day for the 95th percentile (2.011.2 μg/kg bw/day at the upper bound). These variations in exposure between countries were a
consequence of different consumption patterns, since the same arsenic concentrations were used
as inputs in the exposure assessment.
Xue et al (2010) reported exposure to total arsenic from food in the US based on a Total Diet Study
to be 0.36 μg/kg bw/day at the mean and 1.40 μg/kg bw/day at the 95th percentile. For exposure
from water, they reported 0.03 μg/kg bw/day at the mean and 0.11 μg/kg bw/day at the 95th
percentile. The mean inorganic arsenic exposure from food was 0.05 μg/kg/day.
More recently, the literature on dietary exposure to arsenic in different countries has been
comprehensively reviewed by the World Health Organisation (WHO) (2011a and b). Mean and 95th
percentile inorganic arsenic dietary exposure estimates were summarised for Europe, North
America, South America and Asia. In Europe, adult exposure was estimated at 0.02-0.61 μg/kg
bw/day at the mean, and 0.27-0.99 μg/kg bw/day at the 95th percentile. For children (1-8 years)
exposure estimates were higher, ranging from 0.31 to 1.39 μg/kg bw/day at the mean and 0.612.66 μg/kg bw/day at the 95th percentile. In North America, mean exposure to inorganic arsenic for
the whole Canadian population was estimated at 0.29 μg/kg bw/day. In the US, adult mean
exposure was estimated to be 0.08-0.20 and 0.16-0.34 μg/kg bw/day at the 95th percentile. Mean
exposure of children (1-6 years old) to inorganic arsenic in the US was estimated at 0.12-0.32
μg/kg bw/day.
According to WHO (2011a), exposure to inorganic arsenic in South America (Chile only) was
2.08-21.48 μg/kg bw/day, noting that contaminated water was a contributor to exposure. In Asia
(Bangladesh, China, Taiwan, Japan), mean exposure for adults ranged from 0.24-3.00 μg/kg
bw/day, 0.83-1.29 μg/kg bw/day at the 95th percentile (Japan only).
12
5.3 Risk characterisation
The health risks associated with dietary exposure to inorganic arsenic from the consumption of
seaweed is variable and dependent on the:



concentration of inorganic arsenic in the seaweed consumed
amount of seaweed consumed and whether this is on a regular basis
the consumption of other foods in the diet that also contain inorganic arsenic
If seaweed is consumed that has inorganic arsenic levels below the ML of 1 mg/kg, consumption is
unlikely to have a substantial impact on inorganic arsenic exposure. Consequently, based on the
data currently available, for the overall Australian population the risk of significantly increased
exposure to inorganic arsenic from consumption of seaweed and seaweed products is considered
low. This scenario is likely given the inorganic arsenic levels in the majority of samples tested in
this survey is low and compliant with the requirements in the Code (with the exception of a single
composite sample of hijiki seaweed).
However, there might be some population groups or individuals who consume large amounts of
hijiki seaweed regularly and therefore are more likely to be exposed to high amounts of arsenic
compared with the overall Australian population. These high consuming people may have a higher
potential health risk from exposure to inorganic arsenic than the general population but this risk is
not easily quantifiable. In particular, small children who consume hijiki seaweed regularly may be
at more risk of increased inorganic arsenic exposure from seaweed than other age groups
because of their low bodyweight and resultant higher amount of food consumed per kilogram
bodyweight.
The JECFA Committee (WHO 2011a) noted in its evaluation that there was considerable
uncertainty regarding the magnitude of the calculated BMDL0.5 (3 μg/kg bw/day; range - 2–7 μg/kg
bw/day) and whether it could readily be extrapolated to populations other than those is Asia, where
the epidemiological studies were undertaken, due to uncertainties around the influence of
nutritional status, such as low protein intake, and other lifestyle factors on observed outcomes. The
additional risk arising from a small increase in exposure through seaweed consumption in Australia
is difficult to estimate but given the uncertainties surrounding the BMDL0.5 identified by JECFA, it
seems unlikely to appreciably alter the risk for consumers.
6 Risk management activities
In response to the findings from this survey, the relevant jurisdiction that supplied the hijiki
seaweed sample was notified of the result for further investigation and/or any follow-up activity.
DAFF was also notified of the survey findings.
For border testing of imported food, hijiki seaweed is classified as a risk category food, given the
possibility of high concentrations of inorganic arsenic. Hijiki seaweed, from a new producer
exporting to Australia, is initially referred to DAFF by Customs at a rate of 100% of consignments,
and is tested to ensure inorganic arsenic levels do not exceed the ML in the Code of 1 mg/kg (at
85% hydration). Once five consecutive consignments from the producer of the specific food have
passed inspection, the inspection rate is reduced to 25%. After a further 20 consecutive passes,
the inspection rate is reduced to 5%. Any subsequent consignments that fail result in a return to
100% testing of that product from that producer until a history of compliance is re-established for
the food. Consignments of risk food which fail inspection cannot be imported. These foods are reexported or destroyed.
In recent years, the rate of compliance of inorganic arsenic in imported hijiki seaweed has been
high, at 100% (n=10) for the period of July to December 2010 (AQIS 2010). Before this, the last
report of non-compliance was in the period of July 2006-June 2007, where two consignments failed
13
(AQIS 2007). This recent high compliance of imported hijiki seaweed with the ML for inorganic
arsenic is reassuring for Australian consumers of imported hijiki seaweed.
In 2011, additional measures were implemented at the Australian border for hijiki seaweed. This
has involved updating the description of hijiki seaweed in the DAFF risk food category to also
encompass scientific names and synonyms, recognising the variation in labelling used for this type
of seaweed. According to this description, hijiki seaweed is also known as Hizikia fusiforme,
Sargassum fusiforme, Hizikia fusiformis, Hiziki, Mehijiki, Hoshi hiziki, Deer tail grass, Sheep nest
grass and Horsetail tangle. Interestingly, products labelled as both hijiki and Sargassum fusiforme
were analysed in this study; however the concentrations of inorganic arsenic varied by at least 20fold (Tables 1 and 3). This difference in concentration is consistent with the concentration ranges
demonstrated for hijiki seaweed in Table 3. Hijiki seaweed is harvested from the lower end of the
eulittoral and upper sublittoral zone where arsenic levels are variable and are influenced by
seasonal changes and geochemical composition. Therefore, it is possible that the two seaweed
samples are of the same species but were harvested from different regions and/or at different
times of the year (FAO 2003; Gupta and Abu-Ghannam 2011; Borak and Hosgood 2007).
There are also difficulties associated with identifying seaweed species, particularly for seaweed
that is imported in the original packaging and re-labelled in English for sale in Australia (NSWFA
2010). A considerable amount of seaweed is imported into Australia (e.g. approximately 5,500
tonnes in 2011), mainly from China, Japan, Korea and Ireland (RIRDC 2010; ABS 2011). It is
possible that some of these products may have been incorrectly labelled. Given the number of
synonyms for a single seaweed species, any conclusions comparing these samples should take
this into consideration. For further information on alternative names for brown seaweed, please
refer to the FSANZ website at:
http://www.foodstandards.gov.au/scienceandeducation/factsheets/factsheets/adviceonbrownseawe
edforpregnantwomenbreastfeedingwomenandchildren27june2011/brownseaweedstable.cfm
FSANZ considers that existing risk management measures, i.e. the ML in the Code and testing at
the border, for hijiki seaweed are suitably protective of the health and safety of the Australian
population. However, the dietary exposure of the Australian population to organic and inorganic
arsenic in food will continue to be investigated by FSANZ and included in the upcoming 25th ATDS.
The suitability of risk management measures will be further reviewed following completion of the
25th ATDS.
Further studies may be necessary to better understand the variability of arsenic concentrations in
specific foods due to a number of factors, such as the geology of the region in which foods are
grown and different varieties. Information about seaweed consumption data for different population
groups in Australia would also be useful for the purposes of the dietary exposure assessment.
Contemporary food consumption data will become available in the future through the 2011-13
Australian Health Survey, which is currently being conducted by the Australian Bureau of Statistics.
14
7 Risk communication
FSANZ has reviewed and updated the factsheet for consumers regarding arsenic in food, which is
available on the FSANZ website at:
http://www.foodstandards.gov.au/consumerinformation/arsenic.cfm
The factsheet contains information on seaweed, iodine, arsenic, a summary of the current survey
findings and risk management measures.
FSANZ will update its advice to consumers through the factsheet following completion of the 25th
ATDS and other possible studies, or as additional information becomes available.
8 Conclusion
Overall, this report suggests that levels of inorganic arsenic in most seaweed available in Australia
are below the regulatory limit, with the notable exception of one composite hijiki seaweed sample.
This composite is comprised of individual samples of the same brand, so conclusions cannot be
drawn as to whether this finding is representative of all hijiki seaweed available in Australia. DAFF
continues to monitor inorganic arsenic levels in hijiki seaweed imported into Australia for
compliance with the Code.
In general, the consumption of seaweed and seaweed products in the Australian population is
likely to be low and the resulting contribution to total dietary exposure to inorganic arsenic is
therefore likely to be small for the general population. Population groups and individuals who have
a high exposure to arsenic from other sources in the diet, and also regularly consume hijiiki
seaweed, should be aware that they may have a higher potential health risk from exposure to
arsenic than the general population.
9 Acknowledgements
FSANZ would like to acknowledge the following organisations and people:
 Officers from each state and territory food regulatory agency for the collection of
samples and their dispatch to the laboratory.
 The National Measurement Institute for the preparation and analysis of samples.
15
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18
APPENDIX 1
Appendix 1: Dietary Exposure Assessment
1.
Background
In this survey, FSANZ found that seaweeds are a potential source of arsenic exposure that had not
been included in the dietary exposure estimates for total arsenic in the 23rd ATDS. Using the
dietary exposure estimates for total arsenic from the 23rd ATDS as a baseline, FSANZ considered
a range of possible scenarios to describe potential additional dietary exposure to inorganic arsenic
for individual consumers of seaweed based food.
2.
Assumptions
The 23rd ATDS reported average exposure (mean) and high consumers6 exposure (90th percentile)
to total arsenic, which were considered the populations of interest for this assessment. Exposures
reported were the same for the whole population and consumers because all respondents
consumed foods that were potential sources of arsenic exposure. Upper bound and lower bound
dietary exposures reported in the 23rd ATDS were very similar for total arsenic. Therefore, the
upper bound mean and 90th percentile of exposure only were selected as the baselines (Table A1,
expressed as mg/day) to which potential exposure from seaweed (including all seaweed products)
was added. Using these baselines ensures that the assessment is sufficiently protective of high
consumers.
The same age groups used in the ATDS were used in this assessment with the exception of
9-month-olds who were not included because it was considered highly unlikely that this age group
would consume seaweed or seaweed products.
FSANZ has no suitable data on seaweed consumption. Based on FSANZ’s understanding of
current typical Australian consumption patterns, seaweed is unlikely to be widely or regularly
consumed by very young children and across the wider population, with the possible exception of
sushi nori. In the absence of such consumption data at an individual level, FSANZ has assumed
that all population groups would consume the equivalent of 10 g of dried seaweed per day, an
amount that is likely to be an upper level of consumption. This approach is consistent with the
assumptions made by EFSA when estimating the potential contribution to inorganic arsenic
exposure from seaweed (EFSA 2009). The data for inorganic arsenic content of seaweed used in
this assessment has been restricted to that reported in Table 1 (see above), using the overall
median and maximum inorganic arsenic concentrations for dried seaweed of 0.16 and 7.80 mg/kg
respectively to construct exposure scenarios.
Considering the lack of representative speciation data for seaweed and other foods, it was not
possible to use inorganic arsenic concentration data as an input for dietary exposure estimates. No
typical ratios for organic versus inorganic arsenic content of seaweeds or the wider food supply
were readily available. Consequently, the proportion of inorganic to total arsenic was assumed to
vary from 50-100% in different scenarios, with 70% considered to be an estimate of the overall
average. A similar approach was followed by EFSA in their review of arsenic in 2009 (EFSA 2009).
Mean bodyweights of the population groups were calculated based on the values reported in the
1995 National Nutrition Survey (NNS) for adults (unweighted) and 2007 Australian National
Children’s Nutrition and Physical Activity Survey (ANCNPAS) (weighted) which formed the basis
for the exposure estimates reported for the 23rd ATDS (Table A2).
6
Consumers are defined as the consumers of foods containing the chemical of interest
19
APPENDIX 1
Table A1 Mean and 90th Percentile exposures to total arsenic reported in the 23rd ATDS
Population
distinct count
(number)†
weighted
count
(number)‡
Dietary Exposure (mg/d)
Ratio
consumers/
respondents¥
Mean
90thpercentile
2007 Australian National Children’s Nutrition and Physical Activity Survey (ANCNPAS)
2-5 years
6-12 years
13-16 years
1,566
1,606
1,315
1,178
2,090
1,219
100
100
100
Not weighted
100
0.025
0.032
0.037
0.058
0.073
0.086
0.041
0.084
1995 National Nutrition Survey (NNS)
17+ years
11,129
†
‡
Distinct count is the number of actual consumers in the survey (sample population), Weighted count is where some
consumers contribute more or less than others to make each contribution more representative of the actual population,
¥
Ratio consumer to respondent is where the respondent count is divided by the consumer count. In this case, all
respondents are consumers.
Table A2 Mean bodyweights used in dietary exposure estimates for this assessment
Age group
2-5
6-12
13-16
17+
3.
Survey
2007 ANCNPAS
2007 ANCNPAS
2007 ANCNPAS
1996 NNS
mean bw (kg)
18
36
61
74
Weighted




Dietary exposure estimates for different scenarios
There are a number of possible scenarios that can be constructed based on assumptions about
the possible baseline dietary exposure to arsenic (mean or 90th percentile), the concentration of
arsenic in the seaweed, the proportion of inorganic arsenic present in the food and the
consumption amounts of seaweed. Assuming all seaweed consumption (including all seaweed
products) was 10 g/day (dry weight) and a background exposure at the upper bound for all
populations, 12 exposure scenarios were constructed (Table A3). The four scenarios shown in
bold were selected for reporting in Table A4 for all population groups. Scenario 3 presents a ‘best
case’, Scenario 10 a ‘worst case’ and Scenarios 5 and 8 are more ‘typical cases’, i.e. cases that
fall between the best and worst case scenarios. All twelve scenarios were calculated for the most
vulnerable population (children aged 2-5 years) and compared to background exposures.
Table A3 Inorganic arsenic exposure scenarios
Background
Arsenic concentration
in Seaweed
Mean Exposure
median
maximum
median
maximum
90th Percentile exposure
% inorganic in all foods that contribute
to exposure
100
70
50
Scenario 1
Scenario 2 Scenario 3
Scenario 4
Scenario 5 Scenario 6
Scenario 7
Scenario 8 Scenario 9
Scenario 10
Scenario 11 Scenario 12
All respondents consumed foods that were potential sources of arsenic exposure.
20
APPENDIX 1
Table A4 Estimated dietary exposure to inorganic arsenic in four selected scenarios
Scenario 3:
‘best case’
50% inorganic
arsenic
Population
2-5
6-12
13-16
17+
Scenario 5
70% inorganic
arsenic
Seaweed:
Seaweed: median
maximum
concentration
concentration
Mean background exposure
Exposure µg/kg bodyweight/day:
0.7
4.0
0.5
2.1
0.3
1.3
0.3
1.1
Scenario 8
Scenario 10:
‘worst case’
70% inorganic
100% inorganic
arsenic
arsenic
Seaweed:
Seaweed: median
maximum
concentration
concentration
90th Percentile background
2.3
1.5
1.0
0.8
7.6
4.2
2.7
2.2
The estimated dietary exposure to inorganic arsenic including that from seaweed for Scenarios 3,
5, 8 and 10 are shown in Table A4. For the population group aged 2-5 years, exposure varied from
0.7-7.6 µg/kg bw/day, depending on the scenario. For 6-12 year olds and 13-16 year olds,
exposure varied from 0.5-4.2 µg/kg bw/day and 0.3-2.7 µg/kg bw/day respectively. For adults, the
range was 0.3-2.2 µg/kg bw/day.
For the ‘best case’ scenario, exposure ranged from 0.3-0.7 µg/kg bw/day across different
population groups and for the worst case scenario, from 2.2 to 7.6 µg/kg bw/day. Exposure
scenarios are most sensitive to the presence of high arsenic concentrations in seaweed rather than
the background exposure to arsenic as it was estimated in the 23rd ATDS. For example, from Table
A4, assuming 70% of arsenic species are inorganic, estimated exposure is higher in the scenario
that assumes a maximum concentration of arsenic species in the seaweed and mean background
exposure (Scenarios 5) compared to the scenario that assumes a median concentration and 90th
percentile background exposure (Scenario 8).
Figures A1a and A1b show the potential exposure to inorganic arsenic of 2-5 year old children
under the 12 possible scenarios set out in Table A3. Figure A1a shows scenarios based on arsenic
background exposure at the mean and Figure A1b shows scenarios based on the 90th percentile of
background exposure. The bars on the far left of each set of charts show the estimated exposure
to inorganic arsenic excluding seaweed, i.e. the background exposure.
In both charts it can be seen that estimated dietary exposure to inorganic arsenic without seaweed
(background, bars to the left) is quite similar to exposure when seaweed is included under the
assumption that inorganic arsenic is present at the median concentration reported in this survey
(bars in the centre). In contrast, if seaweed is assumed to have inorganic arsenic concentrations at
the maximum reported in this survey potential dietary exposure is far higher than the background
(bars at the right).
21
A
APPENDIX
1
Figure A1 Estimated dietary exp
posure of 2--5 year old children
c
to inorganic
i
arrsenic assum
ming 50,
70 and 100
0% of arsen
nic species are inorgan
nic and seaw
weed conce
entration off arsenic is zero,
z
at the
median (0..16 mg/kg) or
o maximum
m (7.8 mg/kkg).
(a) Backgrround expos
sure at the mean
m
(averrage consum
mers)
ntile (high consumers)
c
(b) Backgrround expossure at the 90th percen
22
APPENDIX 1
4.0
Uncertainty analysis
4.1
Assessment objectives
FSANZ has surveyed inorganic arsenic in seaweed and seaweed-containing products available in
Australia to assess the public health risks associated with the presence of inorganic arsenic in
seaweed and seaweed products. The objective was to provide risk managers with the assessment
of the risks to public health and safety including an exposure assessment using data currently
available.
4.2
Exposure scenarios and input parameters
4.2.1
Uncertainty associated with concentration data
There are several areas of potential uncertainty in dietary exposure estimates. For example, it is
uncertain whether the available concentration data is representative of the inorganic arsenic
concentration in seaweeds. There is not enough data on the presence of organic and inorganic
arsenic species in foods that are major contributors to arsenic exposure, such as rice. There is
almost no available data on seaweed consumption (amounts and types) in Australia or the dietary
consumption patterns of population groups that are high consumers of seaweed.
The quality of the occurrence data is expected to be good and the uncertainty in the values is
considered to be low. The analyses were performed by an accredited laboratory using a validated
method of analysis. Based on this method, it is possible that low levels of MMA (an organic form of
arsenic with toxicological significance) may also be present. However, for the purposes of this
report, a conservative approach has been taken and the possible presence of organic MMA has
been included in the total inorganic arsenic concentration. This may result in an overestimate of
the total inorganic arsenic levels in seaweed due to the uncertainty of the contribution of the MMA.
For the dietary exposure estimates, maximum and median concentrations were used as inputs.
Upper bound and lower bound exposures for baseline exposure were very similar; therefore, the
upper bound mean and 90th percentile of exposure only were selected as the baselines indicating
the decision on how to treat non detect results for seaweed samples below the LOR was not a
critical factor in contributing to uncertainty of results.
4.2.2
Uncertainty associated with food consumption data
The food consumption amounts used as inputs for the exposure baseline were based on 24 hour
recall data. In some cases, this type of data is expected to underestimate the number of
consumers of a given food on a long term basis, but this is not relevant for this assessment as all
respondents were consumers of foods containing arsenic. In the absence of other information, the
consumption of seaweed was assigned a value based on an understanding of consumption of
foods containing seaweed, such as soups, chips and salads. The value was consistent with
approaches taken by other risk assessors such as EFSA. It is uncertain if this value represents an
over or underestimate of long term usual consumption of seaweed for some population groups.
However, it is most likely that it represents an overestimate of usual consumption for the general
Australian population.
The overall uncertainty in the dietary exposure estimations is considered to be medium to high. It
most likely represents an overestimate of exposure for the general population but it is not possible
to decide if it results in an over or underestimate of exposure for population groups that are high
consumers of foods with high levels of inorganic arsenic.
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